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A Phenotypic Comparison of Communication-Relevant Domains Between Youth with Down Syndrome and Fragile X Syndrome

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A Phenotypic Comparison of Communication-Relevant Domains Between Youth with Down Syndrome and Fragile X Syndrome ORIGINAL RESEARCH published: 01 October 2018 doi: 10.3389/fgene.2018.00424 Specificity: A Phenotypic Comparison of Communication-Relevant Domains Between Youth With Down Syndrome and Fragile X Syndrome Laura del Hoyo Soriano 1,2*, Angela John Thurman 1,2 and Leonard Abbeduto 1,2 1 MIND Institute, University of California, Davis, Sacramento, CA, United States, 2 Department of Psychiatry and Behavioral Sciences, University of California, Davis, Sacramento, CA, United States Despite the shared presence of an intellectual disability (ID), there is a growing literature documenting important phenotypic differences between Down syndrome (DS) and fragile X syndrome (FXS). These conclusions, however, are based on a synthesis across studies, each of which typically includes only measures of a limited number of constructs, and with differing participant characteristics. Firmer conclusions regarding specific Edited by: phenotypes require a single comprehensive multi-domain assessment of participants Manuel Mattheisen, with the syndrome groups being well matched on chronological age (CA) and cognitive Universitätsklinikum Würzburg, Germany functioning. The current study was designed to fill this gap by assessing several Reviewed by: important cognitive and behavioral domains relevant to communication, such as: Juko Ando, structural language skills, false belief understanding, as well as pragmatics and behavioral Keio University, Japan difficulties, in 30 adolescents of both sexes with DS and 39 males with FXS, matched on Baptiste Couvy-Duchesne, University of Queensland, Australia CA and nonverbal (NV) cognition. After statistically controlling for NV cognition, we did *Correspondence: not find significant syndrome differences in expressive and receptive structural language Laura del Hoyo Soriano or false belief understanding. In contrast, participants with DS displayed less stereotyped [email protected] language and fewer behavioral difficulties compared to males with FXS. Within-syndrome Specialty section: associations among the targeted domains are described. Finally, females with DS This article was submitted to were less impaired than males with DS in almost all structural language domains, Behavioral and Psychiatric Genetics, whereas no significant sex-related differences were observed in NV cognition, false belief a section of the journal Frontiers in Genetics understanding, pragmatics, or behavior. Clinical and methodological implications of the Received: 05 April 2018 findings are discussed. Accepted: 10 September 2018 Published: 01 October 2018 Keywords: Down syndrome, fragile X syndrome, phenotype, language, communication, false belief understanding, behavior Citation: del Hoyo Soriano L, Thurman AJ and Abbeduto L (2018) Specificity: A INTRODUCTION Phenotypic Comparison of Communication-Relevant Domains Down syndrome (DS) is typically caused by an extra copy of all or part of chromosome 21 Between Youth With Down Syndrome and Fragile X Syndrome. (Patterson, 2007). It is the most common known genetic cause of intellectual disability (ID) and, Front. Genet. 9:424. except in relatively infrequent cases of translocations, DS is not inherited (Grieco et al., 2015). doi: 10.3389/fgene.2018.00424 Fragile X syndrome (FXS)-the leading inherited cause of ID- is caused by the expansion of a CGG Frontiers in Genetics | www.frontiersin.org 1 October 2018 | Volume 9 | Article 424 del Hoyo Soriano et al. Phenotypic Comparison Between DS and FXS trinucleodide repeat located in the FMR1 gene on the long arm of Males with FXS also demonstrate structural language the X chromosome (Saldarriaga et al., 2014). Despite the presence production impairments relative to CA expectations. However, of an ID and, therefore, increased risk of communication findings are somewhat mixed as to whether their skills in this impairment in both conditions (Abbeduto and Hagerman, domain are more delayed than expected based on level of 1997; Foley et al., 2015), important phenotypic differences have cognitive functioning (Roberts et al., 2007a; Kover and Abbeduto, been observed between DS and FXS. For example, challenging 2010; Estigarribia et al., 2011). Some studies comparing males behavior and pragmatic (i.e., social) language problems appear to with FXS to cognitively matched typically developing (TD) be more common or severe in FXS, whereas structural language children, show expressive and receptive grammar and vocabulary deficits (e.g., syntactic), although present in FXS, are greater in consistent with mental age (MA) expectations (Abbeduto et al., DS (Abbeduto and Hagerman, 1997; Chapman and Hesketh, 2003; Price et al., 2007; Roberts et al., 2007d; Finestack and 2000; Abbeduto and Chapman, 2005; Abbeduto et al., 2007; Abbeduto, 2010). In contrast, other studies show significantly Finestack et al., 2009; Finestack and Abbeduto, 2010). Social- poorer structural language skills in males with FXS relative to cognitive impairments, which contribute to communicative younger TD children with similar NV MAs (Roberts et al., difficulties, seem to be comparable in degree across the two 2007a; Price et al., 2008; Martin et al., 2013). In addition, syndromes, although the types of errors made in social-cognitive conductive hearing loss associated with recurrent otitis media processing may be specific to each etiology (Abbeduto et al., 2001; is often observed in individuals with FXS and may contribute Cornish et al., 2005). to problems with the structural aspects of expressive language It is important to recognize, however, that most cross- (Barnes et al., 2009), just as in the case of DS (Stoel-Gammon, syndrome studies have assessed only a few domains of 2001). functioning and often have not controlled for other relevant Direct comparisons of structural language difficulties between differences between the syndromes, such as cognitive ability. DS and FXS have been relatively infrequent, and the findings Moreover, participant characteristics, such as chronological age inconsistent across studies. Some studies have not shown (CA) and sex, have differed across study samples. The current differences between the two conditions (Hogan-Brown et al., study was designed to fill the gaps in our knowledge of the 2013), whereas several other studies suggest that those with FXS syndrome-specific phenotypic profiles of DS and FXS, after have better syntactic skills, both receptively and expressively, than matching/controlling for CA and nonverbal (NV) cognition, by their cognitively matched peers with DS (Price et al., 2007, 2008; assessing several important cognitive and behavioral domains Finestack and Abbeduto, 2010). related to communication, including structural language, social Regarding social cognition, most of the studies performed cognition, pragmatic skills and behavioral difficulties in 30 in individuals with FXS or DS have generally focused on adolescents of both sexes with DS and 39 males with FXS. It is impairments in their Theory of Mind (ToM)—the “theory” that important to note that because FXS is an X-linked condition, other people have intentions, thoughts, beliefs and emotions, and females with FXS are, as a group, less severely affected than that these various epistemic states influence people’s behavior males (Hagerman et al., 1992). More specifically, although and how they interact with others, as well as an understanding there is a wide range of functioning observed, depending on that other people’s epistemic states can differ from one’s own the proportion of active cells that have the non-affected X (Carpendale et al., 2007). With regard to DS, there is paucity chromosome (Loesch et al., 2004; Ligsay and Hagerman, 2016), of research on ToM, perhaps reflecting the assumption that less than a third of females with FXS have an ID, making a children with DS have relatively strong social skills. However, comparison with females with DS (or even males with FXS) recent studies have shown that children and adolescents with DS difficult to interpret. Thus, females with FXS were excluded from exhibit problems relative to CA expectations with higher-order the present study. cognitive processing of social information affecting interpersonal Regarding language skills, there is considerable research understanding (Fidler, 2006; Cebula et al., 2010). documenting that structural language skills (i.e., syntax, In the case of those with FXS, it has been well documented that vocabulary, phonology) constitute one of the most impaired males with FXS are impaired relative to CA expectations with aspects of the cognitive profile of individuals with DS. Indeed, regard to ToM, having difficulties in differentiating appearance expressive syntax is especially impaired, with performance from reality (Cornish et al., 2005). In addition, males with co- lagging relative to both NV cognitive and vocabulary level- morbid FXS and autism spectrum disorder (ASD) have greater expectations (Finestack and Abbeduto, 2010; Channell et al., deficits than those with FXS alone (Lewis et al., 2006); however, 2015; Lee et al., 2017). At the same time, there is evidence of it has been suggested that both subgroups of FXS are superior as sex-related variability in structural language skills in the DS regards ToM performance to that of individuals with idiopathic population, with females displaying a longer mean length of ASD (Abbeduto and Murphy, 2004). utterance (MLU) in words, and using richer vocabulary and A cross-syndrome comparison study of males with DS and syntax than males from a very young age (Berglund et al., males with FXS (matched
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